Fusarium species are among the most important phytopathogenic and toxigenic fungi. To understand the molecular underpinnings of pathogenicity in the genus Fusarium, we compared the genomes of three phenotypically diverse species: Fusarium graminearum, Fusarium verticillioides and Fusarium oxysporum f. sp. lycopersici. Our analysis revealed lineage-specific (LS) genomic regions in F. oxysporum that include four entire chromosomes and account for more than one-quarter of the genome. LS regions are rich in transposons and genes with distinct evolutionary profiles but related to pathogenicity, indicative of horizontal acquisition. Experimentally, we demonstrate the transfer of two LS chromosomes between strains of F. oxysporum, converting a non-pathogenic strain into a pathogen. Transfer of LS chromosomes between otherwise genetically isolated strains explains the polyphyletic origin of host specificity and the emergence of new pathogenic lineages in F. oxysporum. These findings put the evolution of fungal pathogenicity into a new perspective.

Fusarium is a genus of filamentous fungi that contains many agronomically important plant pathogens, mycotoxin producers, and opportunistic human pathogens. Comparative analyses have revealed that the Fusarium genome is compartmentalized into regions responsible for primary metabolism and reproduction (core genome), and pathogen virulence, host specialization, and possibly other functions (adaptive genome). Genes involved in virulence and host specialization are located on pathogenicity chromosomes within strains pathogenic to tomato (Fusarium oxysporum f. sp. lycopersici) and pea (Fusarium ‘solani’ f. sp. pisi). The experimental transfer of pathogenicity chromosomes from F. oxysporum f. sp. lycopersici into a nonpathogen transformed the latter into a tomato pathogen. Thus, horizontal transfer may explain the polyphyletic origins of host specificity within the genus. Additional genome-scale comparative and functional studies are needed to elucidate the evolution and diversity of pathogenicity mechanisms, which may help inform novel disease management strategies against fusarial pathogens.

Pathogens secrete effector proteins and many operate inside plant cells to enable infection. Some effectors have been found to enter subcellular compartments by mimicking host targeting sequences. Although many computational methods exist to predict plant protein subcellular localization, they perform poorly for effectors. We introduce LOCALIZER for predicting plant and effector protein localization to chloroplasts, mitochondria, and nuclei. LOCALIZER shows greater prediction accuracy for chloroplast and mitochondrial targeting compared to other methods for 652 plant proteins. For 107 eukaryotic effectors, LOCALIZER outperforms other methods and predicts a previously unrecognized chloroplast transit peptide for the ToxA effector, which we show translocates into tobacco chloroplasts. Secretome-wide predictions and confocal microscopy reveal that rust fungi might have evolved multiple effectors that target chloroplasts or nuclei. LOCALIZER is the first method for predicting effector localisation in plants and is a valuable tool for prioritizing effector candidates for functional investigations. LOCALIZER is available at http://localizer.csiro.au/.

Epipolythiodioxopiperazines (ETPs) are toxic secondary metabolites made only by fungi. The best-known ETP is gliotoxin, which appears to be a virulence factor associated with invasive aspergillosis of immunocompromised patients. The toxicity of ETPs is due to the presence of a disulphide bridge, which can inactivate proteins via reaction with thiol groups, and to the generation of reactive oxygen species by redox cycling. With the availability of complete fungal genome sequences and efficient gene-disruption techniques for fungi, approaches are now feasible to delineate biosynthetic pathways for ETPs and to gain insights into the evolution of such gene clusters.

Summary: Diseases caused by Fusarium pathogens inflict major yield and quality losses on many economically important plant species worldwide, including cereals. Fusarium crown rot (FCR), caused by Fusarium pseudograminearum , is a cereal disease that occurs in many arid and semi‐arid cropping regions of the world. In recent years, this disease has become more prevalent, in part as a result of the adoption of moisture‐preserving cultural practices, such as minimum tillage and stubble retention. In this pathogen profile, we present a brief overview of recent research efforts that have not only advanced our understanding of the interactions between F. pseudograminearum and cereal hosts, but have also provided new disease management options. For instance, significant progress has been made in the genetic characterization of pathogen populations, the development of new tools for disease prediction, and the identification and pyramiding of loci that confer quantitative resistance to FCR in wheat and barley. In addition, transcriptome analyses have revealed new insights into the processes involved in host defence. Significant progress has also been made in understanding the mechanistic details of the F. pseudograminearum infection process. The sequencing and comparative analyses of the F. pseudograminearum genome have revealed novel virulence factors, possibly acquired through horizontal gene transfer. In addition, a conserved pathogen gene cluster involved in the degradation of wheat defence compounds has been identified, and a role for the trichothecene toxin deoxynivalenol (DON) in pathogen virulence has been reported. Overall, a better understanding of cereal host– F. pseudograminearum interactions will lead to the development of new control options for this increasingly important disease problem. Taxonomy : Fusarium pseudograminearum O'Donnell & Aoki; Kingdom Fungi; Phylum Ascomycota; Subphylum Pezizomycotina; Class Sordariomycetes; Subclass Hypocreomycetidae; Order Hypocreales; Family Nectriaceae; Genus Fusarium . Disease symptoms : Fusarium crown rot caused by F. pseudograminearum is also known as crown rot, foot rot and root rot. Infected seedlings can die before or after emergence. If infected seedlings survive, typical disease symptoms are browning of the coleoptile, subcrown internode, lower leaf sheaths and adjacent stems and nodal tissues; this browning can become evident within a few weeks after planting or throughout plant development. Infected plants may develop white heads with no or shrivelled grains. Disease symptoms are exacerbated under water limitation. Identification and detection : Fusarium pseudograminearum macroconidia usually contain three to five septa (22–60.5 × 2.5–5.5 μm). On potato dextrose agar (PDA), aerial mycelia appear floccose and reddish white, with red or reddish‐brown reverse pigmentation. Diagnostic polymerase chain reaction (PCR) tests based on the amplification of the gene encoding translation elongation factor‐1a (TEF‐1a) have been developed for molecular identification. Host range : All major winter cereals can be colonized by F. pseudograminearum . However, the main impact of this pathogen is on bread ( Triticum aestivum L.) and durum ( Triticum turgidum L. spp. durum (Dest.)) wheat and barley ( Hordeum vulgare L.). Oats ( Avena sativa L.) can be infected, but show little or no disease symptoms. In addition, the pathogen has been isolated from various other grass genera, such as Phalaris , Agropyron and Bromus , which may occur as common weeds. Useful websites : https://nt.ars-grin.gov/fungaldatabases/ ; http://plantpath.psu.edu/facilities/fusarium-research-center ; https://nt.ars-grin.gov/fungaldatabases/ ; http://www.speciesfungorum.org/Names/Names.asp